Genome size scaling through phenotype space.

Abstract

BACKGROUND AND AIMS:

Early observations that genome size was positively correlated with cell size formed the basis of hypothesized consequences of genome size variation at higher phenotypic scales. This scaling was supported by several studies showing a positive relationship between genome size and seed mass, and various metrics of growth and leaf morphology. However, many of these studies were undertaken with limited species sets, and often performed within a single genus. Here we seek to generalize the relationship between genome size and the phenotype by examining eight phenotypic traits using large cross-species comparisons involving diverse assemblages of angiosperm and gymnosperm species. These analyses are presented in order of increasing scale (roughly equating to the number of cells required to produce a particular phenotypic trait), following the order of: cell size (guard cell and epidermal), stomatal density, seed mass, leaf mass per unit area (LMA), wood density, photosynthetic rate and finally maximum plant height.

SCOPE:

The results show that genome size is a strong predictor of phenotypic traits at the cellular level (guard cell length and epidermal cell area had significant positive relationships with genome size). Stomatal density decreased with increasing genome size, but this did not lead to decreased photosynthetic rate. At higher phenotypic scales, the predictive power of genome size generally diminishes (genome size had weak predictive power for both LMA and seed mass), except in the interesting case of maximum plant height (tree species tend to have small genomes). There was no relationship with wood density. The general observation that species with larger genome size have larger seed mass was supported; however, species with small genome size can also have large seed masses. All of these analyses involved robust comparative methods that incorporate the phylogenetic relationships of species.

CONCLUSIONS:

Genome size correlations are quite strong at the cellular level but decrease in predictive power with increasing phenotypic scale. Our hope is that these results may lead to new mechanistic hypotheses about why genome size scaling exists at the cellular level, and why nucleotypic consequences diminish at higher phenotypic scales.

A traditional bivariate scatter plot of two variables, such as genome size and guard cell length (A), will normally include a regression line, and the significance of such a relationship expounded. It is important to note that this is a predictive relationship between x and y, but not an evolutionary prediction, and it violates the assumption that the data are independent because all species share varying degrees of evolutionary relatedness (as depicted for the species in A in the phylogenetic tree presented in D). Independence is achieved by calculating differences in trait values between all sister taxa (one such calculation is highlighted in B). This calculation is performed iteratively across the entire phylogeny essentially transforming the data into n – 1 estimates of evolutionary change, which are then plotted in a new Cartesian space (C). A regression can be calculated from these data representing the unweighted average of all evolutionary changes between two traits. For heuristic purposes, highlighted are divergences at several different taxonomic levels shown in (C) and (D) with the same symbols.

The relationship between genome size and (A) guard cell length, (B) epidermal cell area, (C) stomatal density and (D) mass-based photosynthetic rate (Amass). For D, the data are split into angiosperms (closed circles) and gymnosperms (open circles). At the cellular level, there is a strong positive relationship between 2C DNA content and (A) guard cell length and (B) epidermal cell area. There was also a significant negative relationship between 2C DNA content and (C) stomatal density. At a higher phenotypic scale, there is a weak negative relationship between 2C DNA content and (D) Amass across all seed plants. However, for gymnosperms alone the relationship is significantly negative, whereas for angiosperms alone the slope is nearly zero. See for a more complete statistical description.

The relationship between genome size and (A) seed mass, (B) leaf mass per unit area (LMA), (C) wood density and (D) maximum plant height. The data are split into angiosperms (closed circles) and gymnosperms (open circles). There is a significant positive relationship between 2C DNA content and (A) seed mass across all species. However, the positive relationship was not consistent across congeneric species (each black line corresponds to a congeneric slope). For 2C DNA content and (B) LMA, angiosperms alone have a significant negative relationship, and gymnosperms alone have a significant positive relationship. For 2C DNA content and (C) wood density the significant negative relationship across all species was not maintained within either angiosperms or gymnosperms. For 2C DNA content and (D) maximum plant height, there is a significant negative relationship within angiosperms with large genome angiosperms never being associated with large height. In (D), each grey line corresponds to a different quantile of data to highlight the boundary to the distribution for larger genome sizes. See for a more complete statistical description.